Skip to main content
Log in

Essential Gene Clusters Identified in Stenotrophomonas MB339 for Multiple Metal/Antibiotic Resistance and Xenobiotic Degradation

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Stenotrophomonas MB339, a bacterium, which could potentially utilize aromatic compounds and tolerate different heavy metals was isolated from industrial wastewater. Subsequent experiments revealed strains ability to resist antibiotics ofloxacin, streptomycin, rifampicillin, erythromycin, ampicillin, clindamycin, and toxicants including As2+, Hg2+, Cu2+, Ni2+, Pb2+. The shotgun sequencing strategy, genome assembly and annotation uncovered specific features, which make this strain MB339 effectively promising to cope with highly contaminated conditions. This report presents isolate’s assembled genome and its functional annotation identifying a set of protein coding genes (4711), tRNA (69 genes), and rRNA (9 genes). More than 2900 genes were assigned to various Clusters of Orthologous Groups (COGs) and 1114 genes attributed to 37 different Koyoto Encyclopedia of Genes and Genomes (KEGGs) pathways. Among these annotated genes, eighteen were for key enzymes taking part in xenobiotic degradation. Furthermore, 149 genes have been assigned to virulence, disease, and defense mechanisms responsible for multidrug and metal resistance including mercury, copper, and arsenic operons. These determinants comprised genes for membrane proteins, efflux pumps, and metal reductases, suggesting its potential applications in bioremediation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Altimira F, Yanez C, Bravo G, Gonzalez M, Rojas L, Seeger M (2012) Characterization of copper-resistant bacteria and bacterial communities from copper-polluted agricultural soils of central Chile. BMC Microbiol 12:193

    Article  CAS  Google Scholar 

  2. Alvarez-Ortega C, Olivares J, Martinez JL (2013) RND multidrug efflux pumps: what are they good for? Front Microbiol 4:1–11

    Article  Google Scholar 

  3. Aslam F, Yasmin A, Thomas T (2016) Genome Sequence of Klebsiella quasipneumoniae subsp. similipneumoniae MB373, an effective bioremediator. Genome Announcements 4(5):e01068–e01016

    Article  Google Scholar 

  4. Auch AF, Jan M, Klenk HP et al (2010) Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2(1):117

    Article  Google Scholar 

  5. Aziz RK, Bartels D, Best AA et al (2008) The RAST server: rapid Annotations using Subsystems Technology. BMC Genom 9:75

    Article  Google Scholar 

  6. Bankevich A, Nurk S, Antipov D et al (2012) SPAdes: a new genome assembly alogorithm and its applications to single cell sequencing. J Comput Biol 19:455–477

    Article  CAS  Google Scholar 

  7. Berg G, Roskot N, Smalla K (1999) Genotypic and phenotypic relationship between clinical and environmental isolates of Stenotrophomonas maltophilia. J Clin Microbiol 37(11):3594–3600

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Caliz J, Montserrat G, Marti E et al (2012) The exposition of calcareous Mediterranean soil to toxic concentrations of Cr, Cd and Pb produces changes in microbiota mainly related to toxic differential metal bioavailability. Chemosphere 89(5):494–504

    Article  CAS  Google Scholar 

  9. Cao Y, Fanning S, Proos S, Jordan K, Srikumar S (2017) A review on the applications of next generation sequencing technologies as applied to food-related microbiome studies. Front Microbiol 8:1–16

    Google Scholar 

  10. Chan KG (2016) Whole-genome sequencing in the prediction of antimicrobial resistance. Exp Rev Anti-infect Ther 14(7):617–619

    Article  CAS  Google Scholar 

  11. Chong TM, Yin WF, Chen JW et al (2016) Comprehensive genomic and phenotypic metal resistance profile of Pseudomonas putida strain S13. 1.2 isolated from a vineyard soil. ASM Express 6(1):95–101

    Article  Google Scholar 

  12. Dash HR, Sahu M, Mallick B et al (2017) Functional efficiency of MerA protein among diverse mercury resitance bacteria for efficient use in bioremediation of inorganic mercury. Biochimie 142:207–215

    Article  CAS  Google Scholar 

  13. Deng H, Li XF, Cheng WD, Zhu YG (2009) Resistance and resilience of Cu-polluted soil after perturbation, tested by a wide range of soil microbial parameters. FEMS Microbiol Ecol 70:137–148

    Article  Google Scholar 

  14. Fashola MO, Ngole-Jeme VM, Babalola OO (2016) Heavy metal pollution from gold mines: Environmental effects and bacterial strategies for resistance. Int J Environ Res Public Health 13(11):1047

    Article  Google Scholar 

  15. Franco AR, Calheiros CS, Pacheco CC, De Marco P, Manaia CM, Castro PM (2005) Isolation and characterization of polymeric galloyl-esterdegrading bacteria from a tannery discharge place. Microb Ecol 50:550–556

    Article  CAS  Google Scholar 

  16. Gaudreau C, Gilbert H (1997) Comparison of disc diffusion and agar dilution methods for antibiotic susceptibility testing of Campylobacter jejuni subsp. jejuni and Campylobacter coli. J Antimicrob Chemother 39(6):707–712

    Article  CAS  Google Scholar 

  17. Ghoreishi G, Alemzadeh A, Mojarrad M, Djavaheri M (2017) Bioremediation capability and characterization of bacteria isolated from petroleum contaminated soils in Iran. Sustain Environ Res 27(4):195–202

    Article  CAS  Google Scholar 

  18. Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29(8):1072–1075

    Article  CAS  Google Scholar 

  19. Hasnat A, Rahman I, Pasha M (2013) Assessment of environmental impact for tannery industries in Bangladesh. Int J Environ Sci Develop 4(2):217–220

    Article  Google Scholar 

  20. Hrynkiewicz K, Baum C (2014) Application of microorganisms in bioremediation of environment from heavy metals. In: Environmental deterioration and human health. Springer, Dordrecht, pp. 215–227

    Chapter  Google Scholar 

  21. Huo YY, Li ZY, Cheng H, Wang CS, Xu XW (2014) High quality draft genome sequence of the heavy metal resistant bacterium Halomonas zincidurans type strain B6T. Stand Genomic Sci 9(1):30–39

    Article  Google Scholar 

  22. Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform 11(1):119

    Article  Google Scholar 

  23. Jones P, Binns D, Chang HY et al (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30(9):1236–1240

    Article  CAS  Google Scholar 

  24. Karelova E, Harichova J, Stojnev T, pangallo D, Ferianc P (2011) The isolation of heavy-metal resitant culturable bacteria and resiatance determinants from a heavy-metal-contaminated site. Biologia 66(1):18–26

    Article  CAS  Google Scholar 

  25. Koonin EV (2016) Horizontal gene transfer: essentiality and evolvability in prokaryotes and roles in evolutionary transitions. F1000Research 5:1805

    Article  Google Scholar 

  26. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108

    Article  CAS  Google Scholar 

  27. Li XZ, Plesiat P, Nikaido H (2015) The challenge of efflux mediated antibiotics resistance in gram negative bacteria. Clin Microbiol Rev 28(2):337–418

    Article  Google Scholar 

  28. Lowe TM, Eddy SR (1997) tRNA scan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  CAS  Google Scholar 

  29. Markowitz VM, Chen IMA, Palaniappan K, Chu K, Szeto E, Pillay M, Anderson I (2013) IMG 4 version of integrated microbial genomes comparative analysis system. Nucleic Acids Res 42(1):560–567

    Google Scholar 

  30. Marzan LW, Hossain M, Mina SA, Akhter Y, Chowdhury AMA (2017) Isolation and biochemical characterization of heavy-metal resistant bacteria from tannery effluents in Chittagong city, Bangladesh: bioremediation viewpoint. Egypt J Aquat Res 43(1):65–74

    Article  Google Scholar 

  31. Meyer DD, Santestevan NA, Bucker F et al (2012) Capability of selected bacterial consortium for degrading diesel/biodiesel blends (B20): enzyme and biosurfactant production. J Environ Sci Health Part A 47(12):1776–1784

    Article  CAS  Google Scholar 

  32. Moreno R, Rojo F (2013) The contribution of proteomics to the unveiling of survival strategies used by Pseudomonas putida in changing and hostile environments. Proteomics 13:2822–2830

    CAS  PubMed  Google Scholar 

  33. Paulo LM, Ramiro-Garcia J, von Mourik S, Stams AJ, Sousa DZ (2017) Effect of nickel and cobalt on methanogenic enrichment cultures and role of biogenic sulfide in metal toxicity attenuation. Front Microbiol 8:1–12

    Article  Google Scholar 

  34. Punta M, Coggill PC, Eberhardt RY et al (2012) The Pfam families database. Nucleic Acids Res 40:290–301

    Article  Google Scholar 

  35. Ramos JL, Duque E, Gallegos MT, Godoy P, Ramos-Gonzalez MI, Rajas A, Teran W, Segura A (2002) Mechanisms of solvent tolerance in Gram-negative bacteria. Annu Rev Microbiol 56:743–768

    Article  CAS  Google Scholar 

  36. Richter M, Rossello-Mora R (2009) Shifting the genomic gold standard for prokaryotic species definition. Proc Natl Acad Sci USA 106(45):19126–19131

    Article  CAS  Google Scholar 

  37. Rodriguez-Rojas F, Tapia P, Castro-Nallar E et al (2016) Draft genome sequence of multi-metal resistant bacterium Pseudomonas putida ATH-43 isolated from Greenwich Islands, Antarctica. Front Microbiol 7:1777

    Article  Google Scholar 

  38. Sanchez MB, Hernandez A, Martinez JL (2009) Stenotrophomonas maltophilia drug resistance. Future Microbiol 4(6):655–660

    Article  CAS  Google Scholar 

  39. Selengut JD, Haft DH, Davidsen T et al (2007) TIGRFAMs and genome properties: tools to the assignment of molecular function and biological process in prokaryotic genomes. Nucleic Acids Res 35:260–264

    Article  Google Scholar 

  40. Shekhar SK, Godheja J, Modi DR (2015) Hydrocarbon bioremediation efficiency by five indigenous bacterial strains isolated from contaminated soils. Int J Curr Microbiol App Sci 4(3):892–905

    CAS  Google Scholar 

  41. Sinegani ASS, Younessi N (2017) Antibiotic resistance of bacteria isolated from heavy metal polluted soils with different land uses. J Glob Antimicrob Resist 10:247–255

    Article  Google Scholar 

  42. Sturz AV, Matheson BG, Arsenault W, Kimpinski J, Christie BR (2001) Weeds as a source of plant growth promoting rhizobacteria in agricultural soils. Can J Microbiol 47(11):1013–1024

    Article  CAS  Google Scholar 

  43. Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, Van der Lelie D (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl Environ Microbiol 75(3):748–757

    Article  CAS  Google Scholar 

  44. Tamura K, Skecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetic analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  Google Scholar 

  45. Tran TT, Munita JM, Arias CA (2015) Mechanisms of antibiotic resistance. Daptomycin resistance. Ann N Y Acad Sci 1354(1):32–53

    Article  Google Scholar 

  46. Vos M, Hesselman MC, Beek TA, van Passel MW, Eyre-Walker A (2015) Rates of lateral gene transfer in prokaryotes: high but why? Trends Microbiol 23(10):598–605

    Article  CAS  Google Scholar 

  47. Wang H, Wang J, Yu P, Ge P, Jiang Y, Xu R, Chen R, Liu X (2017) Identification of antibiotic resistance genes in multidrug-resistance Acinetobacter baumannii strain, MDR-SHH02, using whole-genome sequencing. Int J Mol Med 39(2):364–372

    Article  CAS  Google Scholar 

  48. Wattam AR, Gabbard JL, Shukla M, Sobral BW (2014) Comparative genomic analysis at the PATRIC, a bioinformatic resource center. Methods and Protocols, Host-Bacteria Interactions. Humana Press, New York, pp 287–308

    Google Scholar 

  49. Youenou B, Favre-Bonte S, Bodilis J, Brothier E, Dubost A, Muller D, Nazaret S (2015) Comparative genomics of environmental and clinical Stenotrophomonas maltophilia strain with different antibiotic resistance profiles. Genome Biol Evol 7:2484–2505

    Article  CAS  Google Scholar 

  50. Zhou P, Huo YY, Xu L, Wu YH, Meng FX, Wang CS, Xu XW (2015) Investigation of mercury tolerance in Chromohalobacter isrelensis DSM 6768 T and Halomonas zincidurans B6T by comparative genomics with Halomonas xinjiangensis TRM0175 T. Mar Genomics 19:15–16

    Article  Google Scholar 

Download references

Acknowledgements

This work was financially supported by Higher Education Commission of Pakistan under international research support initiative program (IRSIP). The whole genome sequence was done at Romaciotti Centre for Genomics, University of New South Wales, Sydney, Australia.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Azra Yasmin.

Additional information

Nucleotide sequence accession number: This Whole genome project has been deposited into GenBank under the accession no. MSLW00000000. The version described in this paper is version MSLW01000000.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 13 KB)

Supplementary material 2 (XLS 10 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aslam, F., Yasmin, A. & Thomas, T. Essential Gene Clusters Identified in Stenotrophomonas MB339 for Multiple Metal/Antibiotic Resistance and Xenobiotic Degradation. Curr Microbiol 75, 1484–1492 (2018). https://doi.org/10.1007/s00284-018-1549-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-018-1549-2

Navigation